Tuesday, February 17, 2015

How to fly without wings?

In the continuing spirit of recent “how to” posts on this blog (see previous post), it is timely to answer another pressing question. Today we will discuss “How to fly without wings?”. Humanity has been fascinated by this question for very long indeed – likely even longer than the question of how to get into grad school. Although entering grad school might be a first step towards learning to fly.

Various ways to fly without wings have been proposed. An obvious solution is to make wings. This idea appeared early on; in Greek mythology, for example, we have the story of Icarus, who made wings of wax and feathers. Sadly, when he flew too close to the sun the wax melted, and Icarus fell into the ocean and drowned. Nice try, Icarus – better learn how to swim first.
Landscape with the Fall of Icarus, c. 1558, by my favourite painter, Pieter Brueghel de Oude. Icarus is falling into the ocean (bottom right) with wings of feathers secured with wax. The local farmers, shepherds, and fishermen are not impressed by the way Icarus has compromised his evolutionary fitness.
Icarus’ failure reminds us that, gravity being what it is, it is hard to fly without wings without compromising your evolutionary fitness. More generally, it can be tricky to disperse efficiently when you are not very mobile. Studies on natural populations often speculate about the means that dispersal-limited organisms might have used to reach remote places such as inselbergs, islands, or crater lakes, or how such organisms managed to spread across vast geographical ranges. Very often it is argued that transport by birds must have been involved. Alternatively, remote places might have been colonised by good dispersers, and dispersal limitation might only have evolved secondarily. Since good dispersers may carry the genetic material of bad dispersers, it might not even take terribly long for poorly-dispersing ecotypes to evolve. So for Icarus to disperse more effectively, it might have been sufficient to find a partner that did have wings – Nike, the Greek winged goddess of victory, would have been a good choice at the time – and to produce a lot of offspring. Provided that Nike’s functional wing genes were dominant, at least some of their offspring might have been able to fly, thereby spreading Icarus’ genes. But since Icarus never met Mendel nor Nike, and since Greek mythology did not cast any other potential partners with functional wings (the Gorgon sisters being less than desirable mates), things unfortunately did not work out for him.

Still, it does seem a plausible mechanism in nature, as featured in this week’s issue of Molecular Ecology for the salt-marsh beetle Pogonus chalceus, the favourite pet of my colleagues Steven Van Belleghem and Frederik Hendrickx at Ghent University. Steven and Frederik reconstructed the evolutionary history of mtIdh, a gene associated with wing-size polymorphism in P. chalceus. Long-winged individuals (homozygous for the long-winged allele) are able to fly, but short-winged individuals (homozygous for the short-winged allele) are not. Still, the short-winged allele (let’s call it the Icarus allele), which Steven and Frederik found to have evolved only once, has now spread over the whole of Atlantic and Mediterranean Europe, a vast area for such a tiny beetle. This colonisation seemed to have happened relatively rapidly by means of a selective sweep – an evolutionary process that figuratively gives wings to your genes, especially when favoured by selection. Exactly how this evolutionary shift happened is a bit of a mystery, but it is clear that short-winged beetles have not made the same mistake as Icarus. In addition to occasional rides on avian taxis, genetic mechanisms involving long-winged individuals transporting Icarus alleles might have sped up the process.

A) The ancestral long-winged and derived short-winged ecotype of the salt-marsh beetle in their respective non-tidal and tidal habitat. As shown in the picture, these habitat types are sometimes in very close proximity. B) Bayesian mtIdh gene tree covering nearly the entire species range, with lineages associated with the long-winged and short-winged ecotype in red and blue, respectively. C) Distribution of sampled long-winged (in red) and short-winged (in blue) populations in Europe.

Interestingly, these two ecotypes of the salt-marsh beetle are sometimes found in very close proximity (10–20 m) in sympatric mosaics. Short-winged populations live in tidal marshes near the shore, while long-winged individuals tend to avoid that habitat, preferring areas that are more inland. Since the tide comes in twice a day, and because flying is always an option when you have fully developed wings, flying is presumably what long-winged individuals do when their feet get wet. In contrast, there is no escape for the short-winged individuals upon inundation. But since tidal inundations only last six hours, short-wings just trap an air bubble and stay submerged, waiting for better times. This difference in tactics automatically induces partial reproductive isolation between the two types – making wings a magic trait. So, while occasional hybridisation and a selective sweep might be responsible for the rapid spread of the Icarus allele at the regional scale, ecological mechanisms might locally discourage hybridisation, promoting the divergence between short-and long-winged populations.

Steven and Frederik conclude that the adaptive genetic variation underlying the local evolution of short- and long-winged populations has an allopatric origin, confirming that allopatric phases may be important at early stages of speciation with gene flow. But what I believe makes this story even more unique is that the salt marsh beetle system is old enough that we can observe parallel evolution of an adaptive phenotype (the short-winged ecotype), yet young enough that we can trace the evolutionary history back to the original mutation (which seems to have occurred no more than 0.047–0.165 million years ago). Such a comprehensive view on both the origin and the spread of a gene associated with adaptation and ecological speciation is rare indeed. Let’s hope this convinces Icarus to apply for grad school.

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  1. Thanks to Ben Haller for mythological advice!

  2. Hey, I didn't study Greek philosophy and literature for two years for nothing. :->